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  • 1
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    Evolutionary genomics of the cold-Adapted diatom Fragilariopsis cylindrus (2017)
    Nature Research
    In:  Nature, 541 (7638). pp. 536-540.
    Details
    Publication Date: 2021-01-08
    Description: The Southern Ocean houses a diverse and productive community of organisms. Unicellular eukaryotic diatoms are the main primary producers in this environment, where photosynthesis is limited by low concentrations of dissolved iron and large seasonal fluctuations in light, temperature and the extent of sea ice. How diatoms have adapted to this extreme environment is largely unknown. Here we present insights into the genome evolution of a cold-Adapted diatom from the Southern Ocean, Fragilariopsis cylindrus, based on a comparison with temperate diatoms. We find that approximately 24.7 per cent of the diploid F. cylindrus genome consists of genetic loci with alleles that are highly divergent (15.1 megabases of the total genome size of 61.1 megabases). These divergent alleles were differentially expressed across environmental conditions, including darkness, low iron, freezing, elevated temperature and increased CO 2 . Alleles with the largest ratio of non-synonymous to synonymous nucleotide substitutions also show the most pronounced condition-dependent expression, suggesting a correlation between diversifying selection and allelic differentiation. Divergent alleles may be involved in adaptation to environmental fluctuations in the Southern Ocean. © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1038/nature20803
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  • 2
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    Structural Insights Into PfARO and Characterization of its Interaction With PfAIP (2020)
    In:  Journal of Molecular Biology, 432 (4). pp. 878-896.
    Details
    Publication Date: 2021-01-08
    Description: Highlights: • We provide for the first time a crystal structure of a P. falciparum rhoptry protein. • We identify a PfARO interacting protein (PfAIP) and provide an in-depth phylogenetic analysis. • Structure-based mutagenesis, high-resolution microscopy and proximity-based protein identification. Abstract: Apicomplexan parasites contain rhoptries, which are specialized secretory organelles that coordinate host cell invasion. During the process of invasion, rhoptries secrete their contents to facilitate interaction with, and entry into, the host cell. Here, we report the crystal structure of the rhoptry protein Armadillo Repeats-Only (ARO) from the human malaria parasite, Plasmodium falciparum (PfARO). The structure of PfARO comprises five tandem Armadillo-like (ARM) repeats, with adjacent ARM repeats stacked in a head-to-tail orientation resulting in PfARO adopting an elongated curved shape. Interestingly, the concave face of PfARO contains two distinct patches of highly conserved residues that appear to play an important role in protein-protein interaction. We functionally characterized the P. falciparum homolog of ARO interacting protein (PfAIP) and demonstrate that it localizes to the rhoptries. We show that conditional mislocalization of PfAIP leads to deficient red blood cell invasion. Guided by the structure, we identified mutations of PfARO that lead to mislocalization of PfAIP. Using proximity-based biotinylation we probe into PfAIP interacting proteins.
    Type: Article , PeerReviewed
    DOI: 10.1016/j.jmb.2019.12.024
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  • 3
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    Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness (2020)
    MDPI
    In:  Biology, 9 (2). Art.Nr. 30.
    Details
    Publication Date: 2021-01-08
    Description: Diatoms are major primary producers in polar environments where they can actively grow under extremely variable conditions. Integrative modeling using a genome-scale model (GSM) is a powerful approach to decipher the complex interactions between components of diatom metabolism and can provide insights into metabolic mechanisms underlying their evolutionary success in polar ecosystems. We developed the first GSM for a polar diatom, Fragilariopsis cylindrus, which enabled us to study its metabolic robustness using sensitivity analysis. We find that the predicted growth rate was robust to changes in all model parameters (i.e., cell biochemical composition) except the carbon uptake rate. Constraints on total cellular carbon buffer the effect of changes in the input parameters on reaction fluxes and growth rate. We also show that single reaction deletion of 20% to 32% of active (nonzero flux) reactions and single gene deletion of 44% to 55% of genes associated with active reactions affected the growth rate, as well as the production fluxes of total protein, lipid, carbohydrate, DNA, RNA, and pigments by less than 1%, which was due to the activation of compensatory reactions (e.g., analogous enzymes and alternative pathways) with more highly connected metabolites involved in the reactions that were robust to deletion. Interestingly, including highly divergent alleles unique for F. cylindrus increased its metabolic robustness to cellular perturbations even more. Overall, our results underscore the high robustness of metabolism in F. cylindrus, a feature that likely helps to maintain cell homeostasis under polar conditions.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.3390/biology9020030
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  • 4
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    Structure-Based Identification and Functional Characterization of a Lipocalin in the Malaria Parasite Plasmodium falciparum (2020)
    Elsevier
    In:  Cell Reports, 31 (12). p. 107817.
    Details
    Publication Date: 2021-01-08
    Description: Highlights: • Crystal structure of the malaria parasite lipocalin • Comparative analysis of lipocalin superfamily members in alveolate genomes • Localization of PfLipocalin to the parasitophorous vacuole and food vacuole • Reverse genetics reveal PfLipocalin function in oxidative damage control Summary: Proteins of the lipocalin family are known to bind small hydrophobic ligands and are involved in various physiological processes ranging from lipid transport to oxidative stress responses. The genome of the malaria parasite Plasmodium falciparum contains a single protein PF3D7_0925900 with a lipocalin signature. Using crystallography and small-angle X-ray scattering, we show that the protein has a tetrameric structure of typical lipocalin monomers; hence we name it P. falciparum lipocalin (PfLCN). We show that PfLCN is expressed in the intraerythrocytic stages of the parasite and localizes to the parasitophorous and food vacuoles. Conditional knockdown of PfLCN impairs parasite development, which can be rescued by treatment with the radical scavenger Trolox or by temporal inhibition of hemoglobin digestion. This suggests a key function of PfLCN in counteracting oxidative stress-induced cell damage during multiplication of parasites within erythrocytes.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1016/j.celrep.2020.107817
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  • 5
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    Identifying metabolic pathways for production of extracellular polymeric substances by the diatom Fragilariopsis cylindrus inhabiting sea ice (2018)
    Nature Research
    In:  The ISME Journal, 12 (5). pp. 1237-1251.
    Details
    Publication Date: 2021-02-08
    Description: Diatoms are significant primary producers in sea ice, an ephemeral habitat with steep vertical gradients of temperature and salinity characterizing the ice matrix environment. To cope with the variable and challenging conditions, sea ice diatoms produce polysaccharide-rich extracellular polymeric substances (EPS) that play important roles in adhesion, cell protection, ligand binding and as organic carbon sources. Significant differences in EPS concentrations and chemical composition corresponding to temperature and salinity gradients were present in sea ice from the Weddell Sea and Eastern Antarctic regions of the Southern Ocean. To reconstruct the first metabolic pathway for EPS production in diatoms, we exposed Fragilariopsis cylindrus, a key bi-polar diatom species, to simulated sea ice formation. Transcriptome profiling under varying conditions of EPS production identified a significant number of genes and divergent alleles. Their complex differential expression patterns under simulated sea ice formation was aligned with physiological and biochemical properties of the cells, and with field measurements of sea ice EPS characteristics. Thus, the molecular complexity of the EPS pathway suggests metabolic plasticity in F. cylindrus is required to cope with the challenging conditions of the highly variable and extreme sea ice habitat.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1038/s41396-017-0039-z
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  • 6
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    Building a locally diploid genome and transcriptome of the diatom Fragilariopsis cylindrus (2017)
    Nature Research
    In:  Scientific Data, 4 (1). Art.Nr. 170149 (2017).
    Details
    Publication Date: 2021-01-08
    Description: The genome of the cold-adapted diatom Fragilariopsis cylindrus is characterized by highly diverged haplotypes that intersperse its homozygous genome. Here, we describe how a combination of PacBio DNA and Illumina RNA sequencing can be used to resolve this complex genomic landscape locally into the highly diverged haplotypes, and how to map various environmentally controlled transcripts onto individual haplotypes. We assembled PacBio sequence data with the FALCON assembler and created a haplotype resolved annotation of the assembly using annotations of a Sanger sequenced F. cylindrus genome. RNA-seq datasets from six different growth conditions were used to resolve allele-specifc gene expression in F. cylindrus. This approach enables to study differential expression of alleles in a complex genomic landscape and provides a useful tool to study how diverged haplotypes in diploid organisms are used for adaptation and evolution to highly variable environments.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1038/sdata.2017.149
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  • 7
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    Structure of Prototypic Peptide Transporter DtpA from E. coli in Complex with Valganciclovir Provides Insights into Drug Binding of Human PepT1 (2019)
    ACS (American Chemical Society)
    In:  Journal of the American Chemical Society, 141 (6). pp. 2404-2412.
    Details
    Publication Date: 2021-01-20
    Description: Members of the solute carrier 15 family (SLC15) transport di- and tripeptides as well as peptidomimetic drugs across the cell membrane. Structures of bacterial homologues have provided valuable information on the binding and transport of their natural substrates, but many do not transport medically relevant drugs. In contrast, a homologue from Escherichia coli, DtpA (dipeptide and tripeptide permease), shows a high similarity to human PepT1 (SLC15A1) in terms of ligand selectivity and transports a similar set of drugs. Here, we present the crystal structure of DtpA in ligand-free form (at 3.30 Å resolution) and in complex with the antiviral prodrug valganciclovir (at 2.65 Å resolution) supported by biochemical data. We show that valganciclovir unexpectedly binds with the ganciclovir moiety mimicking the N-terminal residue of a canonical peptide substrate. On the basis of a homology model we argue that this binding mode also applies to the human PepT1 transporter. Our results provide new insights into the binding mode of prodrugs and will assist the rational design of drugs with improved absorption rates.
    Type: Article , PeerReviewed
    Format: text
    Format: text
    DOI: 10.1021/jacs.8b11343
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  • 8
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    The impact of temperature on marine phytoplankton resource allocation and metabolism (2013)
    Nature Research
    In:  Nature Climate Change, 3 (11). pp. 979-984.
    Details
    Publication Date: 2021-01-08
    Description: Marine phytoplankton are responsible for ∼50% of the CO2 that is fixed annually worldwide, and contribute massively to other biogeochemical cycles in the oceans1. Their contribution depends significantly on the interplay between dynamic environmental conditions and the metabolic responses that underpin resource allocation and hence biogeochemical cycling in the oceans. However, these complex environment–biome interactions have not been studied on a larger scale. Here we use a set of integrative approaches that combine metatranscriptomes, biochemical data, cellular physiology and emergent phytoplankton growth strategies in a global ecosystems model, to show that temperature significantly affects eukaryotic phytoplankton metabolism with consequences for biogeochemical cycling under global warming. In particular, the rate of protein synthesis strongly increases under high temperatures even though the numbers of ribosomes and their associated rRNAs decreases. Thus, at higher temperatures, eukaryotic phytoplankton seem to require a lower density of ribosomes to produce the required amounts of cellular protein. The reduction of phosphate-rich ribosomes2 in warmer oceans will tend to produce higher organismal nitrogen (N) to phosphate (P) ratios, in turn increasing demand for N with consequences for the marine carbon cycle due to shifts towards N-limitation. Our integrative approach suggests that temperature plays a previously unrecognized, critical role in resource allocation and marine phytoplankton stoichiometry, with implications for the biogeochemical cycles that they drive.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1038/nclimate1989
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  • 9
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    Pfcerli2, a duplicated gene in the malaria parasite Plasmodium falciparum essential for invasion of erythrocytes as revealed by phylogenetic and cell biological analysis (2020)
    In:  bioRxiv .
    Details
    Publication Date: 2021-01-08
    Description: Merozoite invasion of host red blood cells (RBCs) is essential for survival of the human malaria parasite Plasmodium falciparum. Proteins involved with RBC binding and invasion are secreted from dual-club shaped organelles at the apical tip of the merozoite called the rhoptries. Here we characterise P. falciparum Cytosolically Exposed Rhoptry Leaflet Interacting protein 2 (PfCERLI2), as a rhoptry bulb protein that is essential for merozoite invasion. Phylogenetic analyses show that cerli2 arose through an ancestral gene duplication of cerli1, a related cytosolically exposed rhoptry bulb protein. We show that PfCERLI2 is essential for blood-stage growth and localises to the cytosolic face of the rhoptry bulb. Inducible knockdown of PfCERLI2 led to an inhibition of merozoite invasion after tight junction formation. PfCERLI2 knockdown was associated with inhibition of rhoptry antigen processing and a significant elongation of the rhoptries, suggesting that the inability of merozoites to invade is caused by aberrant rhoptry function due to PfCERLI2 deficiency. These findings identify PfCERLI2 as a protein that has key roles in rhoptry biology during merozoite invasion.
    Type: Article , NonPeerReviewed
    Format: text
    DOI: 10.1101/2020.11.26.400549
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    OceanRep: Article in a Scientific Journal - without review
  • 10
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    Direct ex vivo gene expression profiling of malaria patients reveals common virulence gene expression in first-time infected patients and severe cases (2020)
    In:  bioRxiv .
    Details
    Publication Date: 2021-01-08
    Description: Sequestration of Plasmodium falciparum-infected erythrocytes to host endothelium through the parasite-derived PfEMP1 adhesion proteins is central to the development of malaria pathogenesis. PfEMP1 proteins have diversified and expanded to encompass many sequence variants conferring the same array of human endothelial receptor binding phenotypes. Here, we analyzed RNA-seq profiles of parasites isolated from 32 P. falciparum infected travelers returning to Germany. Patients were categorized into either malaria naïve (n=15) or pre-exposed (n=17), and into severe (n=8) or non-severe (n=24) cases. Expression analysis of PfEMP1-encoding var genes showed that severe malaria was associated with PfEMP1 containing the endothelial protein C receptor (EPCR)-binding CIDRα1 domain, whereas CD36-binding PfEMP1 was linked to non-severe malaria outcomes. In addition, gene expression-guided determination of parasite age suggested that circulating parasites from non-severe malaria patients were older than parasites from severe malaria patients. First-time infected patients were also more likely to develop severe symptoms and tended to be infected for a longer period, which thus appeared to select for parasites with more efficient sequestration and therefore more pathogenic PfEMP1 variants.
    Type: Article , NonPeerReviewed
    Format: text
    DOI: 10.1101/2020.11.13.381137
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